Abstract

1 Laboratório de Helmintos Parasitos de Vertebrados, Departamento de Helmintologia, Instituto Oswaldo Cruz, Fio Cruz. Avenida Brasil 4365, Manguinhos, Rio de

Janeiro, 21040-900, Rio de Janeiro, Brasil.

2 Laboratório de Biologia de Helmintos Otto Wucherer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Brasil.

3 CNPq Research fellow.

ORIGINAL ARTICLES / ARTÍCULOS ORIGINALES

Resumen

De octubre de 2006 a marzo de 2008, sesenta ejemplares de lenguado Paralichthys isosceles, fueron capturados en el

litoral del Estado de Rio de Janeiro, Brasil. El presente estudio trata de la identificación taxonómica de los cestodos que

parasitan esta especie de pez, así como el análisis de los índices parasitológicos, los sitios de infección, teniendo en

cuenta la importancia higiénico-sanitaria del hospedero en los mercados brasileños y extranjeros. Cincuenta y seis

(93.3%) de los peces colectados estaban infectados con al menos un ejemplar de metacestodos. Diphyllobotriidea estuvo

representados por plerocercoides de dos especies: Diphyllobothrium sp. 1 (similar a D. latum) en el estómago, la mucosa

del estómago y en el mesenterio y Diphyllobothrium sp. 2 (similar a D. dendriticum) en el intestino, el hígado, el ovario y

la cavidad abdominal. Trypanorhyncha estuvo representados por Grillotia carvajalregorum, en el estómago, intestino,

hígado, ovario, mesenterio, la cavidad abdominal, musculatura abdominal y dorsal, Nybelinia lingualis en el estómago,

la mucosa del estómago, el intestino, mesenterio, la serosa del bazo y la musculatura dorsal, Heteronybelinia nipponica

en el intestino, la serosa del riñón, cavidad abdominal y la musculatura abdominal, Otobothrium sp. en el estómago,

intestino, hígado, mesenterio y la cavidad abdominal. Callitetrarhynchus gracilis y Pterobothrium heteracanthum en la

musculatura abdominal, P. crassicole en la serosa del estómago. Tetraphyllidea estuvo representados por Scolex

pleuronectis en el estómago y el intestino. Observaciones sobre el potencial zoonótico de las especies incluidas en

Diphyllobothriidae y Trypanorhyncha y el papel que desempeñan en materia de inspecciones sanitarias son presentadas.

Este es el primer informe de metacestodos parasitando especímenes de P. isosceles.

Palabras clave: Brasil - Diphyllobothriidea - índices parasitarios - Paralichthys isosceles -

potencial zoonótico - Tetraphyllidea - Trypanorhyncha.

Suggested citation: Felizardo, N. N.; Torres, E.J.L.; Fonseca, G.M.C; Pinto, R.M.; Gomes, C. D. & Knoff, M. 2010. Neotropical

Helminthology, vol. 4, nº 2, pp. 113-125.

113

Key words: Brazil - Diphyllobothriidea - Paralichthys isosceles - parasitological indexes - Tetraphyllidea -

Trypanorhyncha - zoonotic potential.

From October 2006 to March 2008, sixty specimens of Paralichthys isosceles, were captured in the littoral of the State of

Rio de Janeiro Brazil. The present study deals with the taxonomic identification of the cestodes parasitizing this fish

species, as well with the analysis of parasitological indexes, sites of infection, taking into account the hygienic-sanitary

importance of the host in Brazilian and foreign markets. Fifty-six (93.3%) out of the collected fishes were infected with at

least one specimen of metacestodes. Diphyllobothriidea were represented by plerocercoids of two species:

Diphyllobothrium sp. 1 (similar to D. latum) in stomach, stomach mucosa and mesentery and Diphyllobothrium sp. 2

(similar to D. dendriticum) in intestine, liver, ovary and abdominal cavity. Trypanorhyncha, were represented by

Grillotia carvajalregorum, in stomach, intestine, liver, mesentery, abdominal cavity, abdominal and dorsal

musculatures, Nybelinia lingualis in stomach, stomach mucosa, intestine, mesentery, spleen serosa, dorsal musculature,

Heteronybelinia nipponica in intestine, kidney serosa, abdominal cavity and abdominal musculature, Otobothrium sp.

in the stomach, intestine, liver, mesentery and abdominal cavity, Callitetrarhynchus gracilis and Pterobothrium

heteracanthum in abdominal musculature, P. crassicolle in stomach serosa. Tetraphyllidea, were represented by Scolex

pleuronectis in stomach and intestine. Remarks on the zoonotic potential of species included in Diphyllobothriidae and

Trypanorhyncha and the role they play concerning sanitary inspections are presented. This is the first report of

metacestodes parasitizing specimens of P. isosceles.

CESTODES OF THE FLOUNDER PARALICHTHYS ISOSCELES JORDAN, 1890

(OSTEICHTHYES - PARALICHTHYIDAE) FROM THE STATE OF RIO DE JANEIRO, BRAZIL

CESTODOS DEL LENGUADO PARALICHTHYS ISOSCELES JORDAN, 1890

(OSTEICHTHYES - PARALICHTHYIDAE) EN EL ESTADO DE RIO DE JANEIRO, BRASIL

1 2 1

Nilza Nunes Felizardo ; Eduardo José Lopes Torres ; Michelle Cristie Gonçalves Fonseca ;

1,3 1 1*

Roberto Magalhães Pinto ; Delir Corrêa Gomes & Marcelo Knoff

Neotrop. Helminthol., 4(2), 2010

2010 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line

Felizardo et al.Cestodes of the flounder

INTRODUCTION

This paper deals with the continuity of studies

related to the helminth parasites of the flounder,

Paralichthys isosceles Jordan, 1890, an important

fish resource of commercial importance either in

local or overseas markets (Felizardo et al., 2009 a,

b). The present investigation aims at the

identification of cestode species under

Diphyllobothriidea, Trypanorhyncha and

Tetraphyllidea that were found parasitizing this

host as well as to supply data on taxonomy,

parasitological indexes, sites of infection, taking

into account their importance referring to public

health and sanitary inspection.

There are no previous reports of larval cestodes

included in Diphyllobothriidea, Trypanorhyncha

and Rhinebothriidea (= Tetraphyllidea in part)

infecting this host so far. Cestode species related to

the two first orders referred above, are important

when sanitary inspection and collective health are

concerned. Specimens of Diphyllobothrium spp.

are the agents of human diphyllobothriasis and are

found in teleostean fishes, and the transmission

occurs after the ingestion of raw, poor cooked or

improperly frozen fish meat. Diphyllobothrium

latum, D. dendriticum and D. pacificum are the

species that have been referred in South America.

Diphyllobothriidea plerocercoids are registered in

teleostean hosts from the Brazilian coast (Pereira

Jr., 1993; Alves et al., 2004, 2005; Pereira Jr. &

Boeger, 2005; Knoff et al., 2008). In Brazil, several

cases of human diphyllobothriasis were reported

(Knoff et al., 2008), thus reinforcing the

importance of investigations related to the presence

of larval cestodes in the intermediate hosts and

transmission patterns.

Larval stages namely plerocerci and plerocercoids

of Trypanorhyncha that are found in several organs

and in the musculature of teleosteans, the

intermediate hosts, even without zoonotic potential

are responsible for the repugnant aspect of the meat

for the final consumer. Adult worms are recovered

from the gastrointestinal system of elasmobranchs

(Knoff et al., 2002); nevertheless, accidental

human infections by larvae of Trypanorhyncha due

to ingestion of raw fish meat have been reported

(Bates, 1990). Two of the cases were related to

specimens of Hepatoxylon trichiuri (Holten, 1802)

Dollfus, 1942, that were found alive in the feces of

humans in South Africa and Mozambique (Heinz,

1954; Fripp & Mason, 1983); besides, there is a

Okada, 1929, adhered to the soft palate of a man in

Japan (Kikuchi et al., 1981). In September, 2009,

during the I Latin American Meeting on

Helminthiasis, held in Teresópolis, Rio de Janeiro

State, Brazil, there was a personal communication

(Jorge Manuel Cárdenas-Callirgos), about the

finding of a species of Nybelinia Poche, 1926 in the

soft palate of a man in Lima, Peru. In the last

decade, some reports have suggested that, possibly,

species of Trypanorhyncha can provoke allergic

reactions in humans (Rodero & Cuéllar, 1999;

Vásquez-Lopez, 2001, 2002; Gomez-Morales et

al., 2008); this approach certainly will change the

procedures adopted for the processing of fish meat

taking into account helminth infections. Several

results of studies related to the finding of

trypanorhynch cestodes in fishes of the Brazilian

littoral are already available (Cordeiro & Luque,

2004; São Clemente et al., 2004, 2007; Pereira Jr. &

Boeger, 2005; Alves & Luque, 2006; Ferreira et al.,

2006; Pinto et al., 2006; Luque et al., 2008; Dias et

al., 2009, 2010; Oliveira et al., 2009; Porto et al.,

2009).

Plerocercoid Tetraphyllidea larvae present

different morphological types, difficulting their

identification and for this reason, a collective name,

Scolex pleuronectis Müeller, 1788 was proposed

by Chambers et al. (2000), after maintaining the

plerocercoids in vitro, and describing eleven

different types of metacestodes, parasitizing fish

species.

In the life-cycle of these cestodes, teleosteans and

some marine mammals are the second intermediate

hosts whereas elasmobranchs the definitive

(Stunkard, 1977; Scholz et al., 1998; Agustí et al.,

2005; Aznar et al., 2007). Recently, part of the

Tetraphyllidea was reallocated in a new order, the

Rhinebothriidea (Healy et al., 2009). In Brazil,

several teleostean fish species have been found

infected with tetraphylidean metacestodes, mainly

by those referred to as S. pleuronectis and Scolex

sp. (Rego & Santos, 1983; Rego et al., 1983;

Takemoto et al., 1996a, b; Knoff et al., 1997; Palm,

1997; Silva et al., 2000 a, b; Luque et al., 2000,

2008; Luque & Alves 2001; Parraguassú et al.,

2002; Alves et al., 2002a, b, 2003, 2004; Tavares

et al., 2004; Alves & Luque, 2006).

114

From October 2006 to March 2008, sixty

specimens of P. isosceles, measuring 35.0±5.9

cm in length and weighing 625±25.2 g were

obtained from professional fishermen. Fishes

were captured in the littoral of the state of Rio

de Janeiro, Brazil, latitudes 21°15'S-23°23'S,

longitudes 40°29'W-44°28'W. After, they were

carried in isothermal containers with ice to the

Laboratorio de Helmintos Parasitos de

Vertebrados, Instituto Oswaldo Cruz,

Fundação Oswaldo Cruz, Rio de Janeiro to be

investigated for helminths. The identification

of fishes is in accordance with Figueiredo &

Menezes (2000). For recovery procedures,

specimens were eviscerated; the organs and

abdominal musculature were transferred to

individual Petri dishes with a 0.65% NaCl

solution to be examined under a stereoscope

microscope. Whenever necessary, blastocysts

were disrupted to permit the proper

observation of the scolices. The filets, obtained

after an incision from near the opercula to the

insertion of the caudal fin, were observed by

means of a negatoscope. Cestodes were

recovered, fixed, clarified and preserved,

according to Eiras et al. (2006). Classification

of Diphyllobothiidea is based on Kuchta et al.

(2008); that of Trypanorhyncha on Dollfus

(1942, 1960), Carvajal & Rego (1983, 1985),

Palm (1997,1999, 2004), in accordance to the

taxonomy proposed by Campbell & Beveridge

(1994); the classification of Tetraphyllidea

follows Euzet (1994) whereas the cestodes

presently considered under Rhinebothriidea

were referred to after Healy et al. (2009). The

terminology applied to larvae and microtriches

was that indicated by Chervy (2002, 2009),

respectively. Indexes of parasitism referred

here follow Bush et al. (1997). For the study of

plerocercoids, five micrometers thick sections

were stained with haematoxylin-eosin (HE).

Morphological comparison of the samples

presently studied was made with specimens

deposited in the Coleção Helmintológica do

Instituto Oswaldo Cruz (CHIOC), where

RESULTS

representative specimens herein considered were

also included. Measurements were obtained in a

brightfield microscope Olympus BX 41, and are in

millimeters (mm), unless otherwise indicated.

Means are followed by the range in parenthesis.

The number of measured larvae is also indicated in

parenthesis (n). Descriptions, measurements and

drawings are restricted to the poor known

specimens to add data to further identifications.

Drawing was made with the aid of a drawing tube,

and micrographs were made with a digital camera

in a brightfield microscope Zeiss Axiophot. For

scanning electron microscopy (SEM) procedures,

samples were dehydrated in an alcoholic series (50-

100ºGL),critical point dried with CO , coated with

gold and electron micrographied under a JEOL

SM25SII and Zeiss 962 microscope submitted to

30 KVolts. For parasitic indexes, abridgments are:

P = prevalence, I = intensity, MI= mean intensity,

RI = range of infection, A = abundance, MA = mean

abundance. For infection sites, abridgments are:

AC = abdominal cavity, S = stomach, L = liver, I =

intestine, M = mesentery, SM = stomach mucosa,

AM = abdominal musculature, DM = dorsal

musculature, O = ovary, SpS = spleen serosa, StS =

stomach serosa, OS = ovary serosa, KS = kidney

serosa.

An amount of 1,205 larval cestodes were recovered

from the different infection sites. These larvae were

identified as described bellow:

Diphyllobothriidea Kuchta, Scholz,

Brabec & Bray, 2008

Diphyllobothriidae Lühe,1910

Diphyllobothrium Cobbold, 1858

Diphyllobothrium sp. 1

(Fig. 1)

Parasitological indexes: P = 6%, MI = 2.5, RI = 1-6,

MA = 0.16; infection sites: S, M, M.; total of

collected specimens: 10 plerocercoids; deposited

specimens: CHIOC 37335a-c and 37336a-b.

Description (n=4): Plerocercoids with retracted

scolex and hardly observed under light microscope,

anterior extremity with a dorso-ventral swelling

due to the retraction of the scolex, bothridial

grooves present in the scolex reaching up 1/3 of the

MATERIAL AND METHODS

Neotrop. Helminthol., 4(2), 2010

115

body length. Body surface wrinkled, not

segmented and without genital primordium. Body

1.45-2.40 (1.80) long, 0.45-0.57 (0.53) wide.

Scolex 0.35-0.58 (0.46) long, 0.44-0.57 (0.51)

wide. Bothridial groove 0.10-0.18 (0.14) long.

There is a single layer of fibers on the epidermic

longitudinal musculature. Microtriches 2-3.5 (2.3)

µm long, inconspicuous under light microscopy

and only observed in cross sections.

Remarks: Specimens of the sample here analyzed,

are most alike to plerocercoids of those related to D.

latum, that present microtriches 2 µm long, similar

to the observed by Andersen et al. (1987) and

Andersen & Gibson (1989), studying plerocercoids

of several fish species from Europe and North

America.

Diphyllobothrium sp. 2

(Fig. 2)

Parasitological indexes: P = 10%, MI = 1.6, RI = 1 –

2, MA = 0.13; infection sites: AC, I, L, O; total of

collected specimens: 8 plerocercoids; deposited

specimens: CHIOC 37337, 37338a-c and 37339a-

c; examined samples: CHIOC 36873, 36874,

36875 and 36876.

Description (n=4): Plerocercoids with the scolex

partially retracted, frontal glands present only at the

scolex region, body surface wrinkled, segmented,

and with genital primordium present. Body 10.40 -

24 (17.20) long 1.22 - 2 (1.61) wide. Scolex (0.97)

long, (1.22) wide. Bothridial groove (0.10) long.

There are two layers of fibers in the longitudinal

epidermic musculature; parenchymal longitudinal

musculature well developed. Microtriches

conspicuous under light microscopy, 7.5 –15 µm

(11.2 µm) long, and in cross sections.

Remarks: The specimens presently recovered are

very similar to those collected in specimens of

Genypterus brasiliensis Regan, 1903, from the

Brazilian littoral by Knoff et al. (2008), reporting to

plerocercoids of Diphyllobothrium sp., with

microtriches 7.5 – 11.25 µm (10 µm) long,

probably belonging to D. dendriticum, and that also

are in agreement with the description of

plerocercoids reported by Andersen et al. (1987)

and Andersen & Gibson (1989). The

parasitological indexes indicated by Knoff et al.

(2008) in G. brasiliensis (P = 24.3 %, MI= 1.66, RI

= 1 – 7, MA = 0.40), are different from those

presently obtained, except for the similar mean

intensity. Considering that the infection sites

reported by Knoff et al. (2008) were related to the

abdominal cavity, intestine serosa and the

musculature near to the cloaca, two other sites, the

liver and the ovary are now included. These

differences may be due to the ecological habits of

these two fish species.

This is the first occurrence of Diphyllobothrium sp.

plerocercoids parasitizing specimens of P.

isosceles.

Trypanorhyncha Diesing, 1863,

Homeacanthoidea Dollfus, 1942, Tentaculariidae

Poche, 1926

Nybelinia Poche, 1926

Nybelinia lingualis (Cuvier, 1817) Dollfus,1927

Parasitological indexes: P = 57 %, MI = 12.5, RI =

1-28, MA = 7.1; infection sites: S, SM, I, SpS, AM,

DM; total of collected specimens: 427

plerocercoids; deposited specimens: CHIOC

37340, 37341, 37342, 37343a-c and 37344a-b;

examined samples: CHIOC 32568, 34397, 34398,

34399a-d.

Remarks: The morphology of the collected

specimens are in accordance with that described for

larval specimens referred by São Clemente &

Gomes (1989) in the elasmobranchs Mustelus

canis (Mitchill, 1815) and M. schmitti Springer,

Cestodes of the flounder

Figures 1-2. Anterior extremity of plerocercoids. Fig.1.

Diphyllobothrium sp. 1. Scale bar = 200 µm. Fig. 2.

Diphyllobothrium sp. 2. Scale bar = 500 µm.

116

Felizardo et al.

1939, and for the oncotaxy of adults reported by

Gomes et al. (2005) in Isurus oxyrinchus

Rafinesque, 1810; hosts were captured in the

Brazilian coast. The present findings are in

accordance with the statement of Palm (1999)

affirming that Nybelinia lingualis has a wide

geographical distribution and low host specificity.

The larvae of N. lingualis collected now, were

found in several infection sites and among those the

abdominal and dorsal musculature, and inducing an

intense infection in the stomach mucosa, with

macroscopic hemorrhagic lesions.

Paralichthys isosceles is a new host record for N.

lingualis.

Heteronybelinia Palm, 1999.

Heteronybelinia nipponica (Yamaguti, 1952)

Palm, 1999

Synonym: Nybelinia rougetcampanae Dollfus,

1960; Heteronybelinia rougetcampanae (Dollfus,

1960) Palm, 1999.

Parasitological indexes: P = 35%, I = 4.2, RI = 1-26,

MA = 1.5; sites of infection: I, AC, KS, AM; total of

collected specimens: 77 plerocercoids; deposited

specimens: CHIOC 37345, 37346, 37347 and

37348; examined samples: CHIOC 32567a, 34500,

34502, 36424.

Remarks: Most of the specimens presently

collected are very similar, concerning length, to

those of H. nipponica recovered from specimens

Genypterus brasiliensis Regan, 1903 by São

Clemente et al. (2004), and remarkably smaller

than the plerocercoids found in specimens of

Sphyrna zygaena (Linnaeus, 1758) by Knoff et al.

(2004); both hosts were captured in the Brazilian

littoral. Morphometric variation in the size of the

scolex and tentacular hooks in this species had

already been observed by Palm & Walter (2000),

after considering H. rougetcampanae synonymous

of H. nipponica; the species were said to be distinct

on the basis of the different sizes of the related

specimens. In the samples collected now, spiniform

microtriches distributed on the bothrial edges were

observed, as reported for plerocercoids parasitizing

specimens of Menticirrhus americanus (Linnaeus,

1758) and Umbrina canosai Berg, 1895 by Pereira

Jr. & Boeger (2005), and referred to as “cuticular

spines”. These structures were observed in the adult

of H. nipponica, recovered from a specimen of

Sphyrna lewini (Griffith & Smith, 1834) by São

Clemente & Gomes (1992) and in the plerocercoid

of H. nipponica from Carcharhinus signatus (Poey,

1868) by Knoff et al. (2004), all from the Brazilian

coast. Nevertheless, sensory fossette with

microtriches, as reported by Pereira Jr. & Boeger

(2005) were not observed so far. The oncotaxy of

plerocercoids recovered from specimens of P.

isosceles is in accordance with the description of H.

nipponica, since present the typical basal tentacular

armature billhooks, with metabasal just above the

billhooks without uncinate hooks and small bulbs,

different from those observed in specimens of H.

yamaguti (Dollfus, 1960) Palm, 1999, that show,

after the last row of “billhooks”, uncinate hooks

and very enlarged bulbs (Knoff et al., 2004; Palm,

2004).

Paralichthys isosceles is a new host record for H.

nipponica.

Otobothrioidea Dollfus, 1942, Otobothriidae

Dollfus, 1942.

Otobothrium Linton, 1890

Otobothrium sp.

Parasitological indexes: P = 15 %, MI = 1.9, RI = 1-

3, MA = 0.3; sites of infection: AC, I, M, S, L; total

of collected specimens: 17 plerocerci; deposited

specimens: CHIOC 37349, 37350, 37351a-b and

37352; examined samples: CHIOC 36428, 36429,

36430 and 36482.

Description (n=3): Scolex 250-300 µm (274 µm)

long, 162-207 µm (178 µm) wide (without the

appendix). Bothrium 157-187 µm (176 µm) long,

(179 µm) wide. Pars vaginalis 132-195 µm (156

µm) long, bulbs 75-92 µm (80µm) long, 37-50 µm

(42 µm) wide, pars bulbosa 82-100 µm (89 µm)

long, 97-145 µm (114 µm) wide, velum (30 µm)

long and appendix 50-62 µm (56µm) long.

Remarks: Plerocerci of Otobothrium sp. have been

reported in specimens of Balistes vetula (Linnaeus,

1758) from the Brazilian coast by São Clemente et

al. (1995), in the musculature, with no reference to

parasitological indexes. Alves et al. (2005)

although registering a prevalence of 20%, did not

report to infection sites. Plerocerci of O. cysticum

(Mayer, 1842) Dollfus, 1942 were found in

specimens of Scomberomorus maculatus (Mitchill,

1815) and Sphyraena guachancho Cuvier, 1829

Neotrop. Helminthol., 4(2), 2010

117

captured in the Brazilian northeast littoral (Palm,

1997), with prevalence of 18.8% and 25%,

respectively, in the body cavity, and in specimens

of G. brasiliensis by São Clemente et al. (2004)

with prevalence of 17.6%, in the mesentery and

celomatic cavity. During observation of specimens

recovered from G. brasiliensis, the presence of a

lateral bothrial pit and bill-hooks stippled in the

basal armature were observed; these structures are

exclusive to O. propecysticum Dollfus, 1969, and

were referred by Beveridge & Justine (2007), in the

revision of the genus, when considered O. cysticum

as species inquirenda, taking into account the fact

that the tentacular armature and mature specimens

are unknown. Thus, specimens recovered from G.

brasiliensis have to be referred to as O.

propecysticum. In the plerocercum of Otobotrium

sp., from B. vetula, cited by Alves et al. (2005), the

presence of the bothrial pit and extroverted

tentacles could not be observed; for this reason, the

analysis of the oncotaxy and further identification

were not attained. As there is no indication of

deposit referring to the material collected by Palm

(1997), the referred samples were unobserved. The

plerocerci from P. isosceles presented

inconspicuous tentacular hooks, bothridial

structures and bothridial pits and thus, were not

specifically identified.

Paralichthys isosceles is a new host record for

Otobothrium sp.

Pterobothriidae Pintner, 1931, Pterobothrium

(Diesing, 1850).

Pterobothrium heteracanthum Diesing, 1850

Parasitological indexes: P = 1.7%, I = 1, A = 0.017;

site of infection: AM; total of collected specimens:

1 pl ero cer coi d; deposited speci men s:

CHIOC37353; examined samples: CHIOC 31.925

a-b, 33798 a-d, 33799, 33800a-c, 34020a-b.

Remarks: The analysis of the studied specimen

agrees with the description of P. heteracanthum

presented by Campbell & Beveridge (1996).

Pterobothriidae Pintner, 1931 was extensively

revised by these authors that have examined

specimens of P. heteracanthum, recovered from

Micropogonias furnieri (Desmarest, 1823)

captured in the Brazilian coast, referred by São

Clemente (1986), detailing the oncotaxy of the

species. The samples presently collected were also

compared to those recovered from sciaenid hosts,

deposited in the CHIOC (Pereira Jr. & Boeger,

2005), confirming the specific identification.

Paralichthys isosceles is a new host record for this

cestode.

Pterobothrium crassicolle Diesing, 1850

Parasitological indexes: P = 1.7%, I = 4, A = 0.067;

site of infection: StS; total of collected specimens:

4 plerocerci; deposited specimens: CHIOC

37354a-d; examined samples: CHIOC 31926a-b,

33622, 33689, 33690 and 33902a-b.

Remarks: Pterobothrium crassicolle has been

registered in several marine and freshwater fishes

in Brazil (Porto et al., 2009). The morphology of

this cestode species recovered from P. isosceles

agrees with the description of P. crassicolle (São

Clemente, 1986; Rego, 1987; Campbell &

Beveridge, 1996). The morphological comparison

was made with specimens collected in M. furnieri

by São Clemente (1986) and by Pereira Jr. &

Boeger (2005), in Oligoplites palometa (Cuvier,

1832) by Takemoto et al. (1996b), thus confirming

the specific identification.

Paralichthys isosceles is a new host record for P.

crassicolle.

Grillotiidae Dollfus, 1969

Grillotia Guiart, 1927

Grillotia carvajalregorum (Carvajal & Rego,

1983) Menoret & Ivanov, 2009

(Figs.3-6)

Synonymy: Progrillotia dollfusi Carvajal & Rego

1983.

Parasitological indexes: P = 73 %, MI = 11.7, RI

=1-56, MA = 8.6; sites of infection: AC, S, StM, I,

L, AM, DM; total of collected specimens: 514

plerocerci; deposited specimens: CHIOC 37363a-

e; examined samples: CHIOC 32018a (holotype),

32018b-d (paratypes), 33719-33735, 36372,

36373, 36431, 36432, 36519a-b, 36674, 36684 and

36698.

Remarks: Carvajal & Rego (1983) described the

species P. dollfusi on the basis of plerocerci. Pereira

Jr. & Boeger (2005) redescribed the peculiar

armature of the basal region, that presents five

hooks encircling the tentacle, anterior to the first

semicircular row of principal hooks. Menoret &

Ivanov (2009) re-named the species as Grillotia

Cestodes of the flounder Felizardo et al.

118

carvajalregorum, after the finding of adult

specimens recovered from Squatina guggenheim

Marini, 1936, in Argentina. The plerocerci

collected now were compared to those deposited in

the CHIOC obtained in the Brazilian coast and

presenting the same pattern referring to oncotaxy

and microtriches, as observed by Pereira Jr. &

Boeger (2005) e Menoret & Ivanov (2009).

In the present study G. carvajalregorum appeared

with the highest parasitological indexes when

compared to the other species, except for the mean

intensity. High parasitological indexes have been

referred to other hosts from the Brazilian littoral, as

occur in Cynoscion guatucupa (Cuvier, 1830) P =

90.48%, MI = 2683.46, MA = 2427,90, Cynoscion

jamaicensis (Vaillant & Bocourt, 1883) P =

81.67%, MI = 433.45, MA = 353.98; Macrodon

ancylodon (Bloch & Schneider, 1801) P = 96.67%;

MI = 792.21 MA = 765.8 by Pereira Jr. & Boeger

(2005); in Pseudopercis numida Miranda-Ribeiro,

1903 and P. semifasciata (Cuvier, 1829) P= 71%

and 65.2%, MI= 2.8 and 4.7, respectively by

Luque et al. (2008). The infection sites cited by

those authors were the mesentery and celomatic

cavity; presently, in specimens of P. isosceles,

besides these sites, parasites occurred in the

abdominal and dorsal musculatures. Adults of this

cestode reported from S. guggenheim in Argentina,

also appeared with a high prevalence (83%) in the

six investigated hosts (Menoret & Ivanov, 2009).

This is a new host record for G. carvajalregorum.

Poecilacanthoidea Dollfus, 1942,

Lacistorhynchidae Guiart, 1927,

Callitetrarhynchus Pintner, 1931

Callitetrarhynchus gracilis (Rudolphi, 1819)

Pintner, 1931

Parasitological indexes: P = 3.33%, I = 1, MA =

0.033; site of infection: AM; total of collected

specimens: 2 plerocercerci; deposited specimens:

CHIOC 37355 and 37356; examined samples:

CHIOC 31924a-b, 32496, 32564, 33618, 33686,

33687, 33904a-b, 34327, 33328, 34303, 34308,

34509, 35005, 36374, 36433, 36532 and 36669.

Remarks: The morphology of the two specimens of

Callitetrarhynchus gracilis recovered from P.

isosceles is in agreement with previous

descriptions by Dollfus (1942), Carvajal & Rego

(1985) and Palm (2004). This species has been

reported from several Brazilian teleosteans and

elasmobranchs (Luque et al., 2000, 2008; Silva et

al., 2000a, b; Luque & Alves, 2001; Knoff et al.,

2002; Cordeiro & Luque, 2004; São Clemente et

al., 2004, 2007; Pereira Jr. & Boeger, 2005; Alves

& Luque, 2006; Ferreira et al., 2006; Pinto et al.,

2006; Dias et al., 2009). The finding of this species

of Poecilacanthoidea in P. isosceles confirming

previous reports, and also its low host specificity,

since it has been collected from various infection

sites of teleosteans.

Paralichthys isosceles is a new host record for C.

gracilis.

Tetraphyllidea Carus, 1863, Scolex Müeller, 1788

Scolex pleuronectis Müeller, 1788

(Fig. 7)

Parasitological indexes: P = 40 %, MI = 9, RI = 1-

70, A = 3.6; total of collected specimens: 216

plerocercoids; sites of infection: S, I; deposited

Neotrop. Helminthol., 4(2), 2010

Figures 3-6. Plerocercus of Grillotia carvajalregorum,

scanning electron micrographs.

Fig. 3. Scolex, lateral view. Fig. 4. Hooks of basal

armature, bothrial surface. Fig. 5. Distal bothrial

surface, near bothrial groove. Fig. 6. Microtriches on

distal bothrial surface. Scale bars: Fig. 3 = 200 µm; Fig.

4 = 30 µm; Fig. 5 = 5 µm; Fig. 6 = 4 µm.

119

specimens: CHIOC 37357a-b, 37358, 37359,

37360, 37361 and 37362; examined samples:

Scolex pleuronectis CHIOC 31952, 32672, 32673,

32674, 34304, 34309a-b, 34331, 34501, 34502,

34525, 34573, 34709a-b, 36245, 36547, 36554,

36414, 36679, 36689, 37155, 37157 and 37158;

Scolex sp. CHIOC 33331, 33332 a-b, 33333 a-b,

33334 a-c, 33335, 33619, 33688, 36483, 36533,

36540 and 36210.

Description (n=6): Plerocercoids 405-4000 µm

(1810 µm) long, 90-310 µm (197 µm) wide.

Retractile apical myzorhynchus (invaginated), 55-

265 µm (150 µm) long, 70-325 µm (164 µm) wide.

Four bothridia (inverted) divided into numerous

loculi by a single longitudinal septum and several

transverse septa, contained in pouches with 80-365

um (214 µm) long, 5-200 µm (125 µm) wide.

Botridial stalks present.

Remarks: The morphology and morphometrics of

specimens of S. pleuronectis recovered from P.

isosceles present similarities with the scolices of

adults of Echeneibothrium Van Beneden, 1850,

presenting scolex with apical retractile

myzorhynchus anf four pedunculate bothrids

divided into transversal septa along with a single

longitudinal septum, that are characteristic of this

genus. Chambers et al. (2000) remark that in

several species, the morphology related to the

scolex of larval tetraphylids can be different in the

adults. Euzet (1994) includes the species of this

genus in Echeneibothriinae de Beauchamp, 1905.

The morphology of the plerocercoids described

now, is similar to that reported by Chambers et al.

(2000) for the metacestode Type 5 (fig3a, p. 291)

presenting the four evaginated bothridia divided

into numerous loculi by a single longitudinal

septum and several transverse septa, and also the so

called “apical sucker” (= apical myzorhynchus).

Authors suggest that these larvae could be included

in Rhinebothriinae Euzet, 1953, in one of the

gen era : R hin ebo thr ium L int on 188 9,

Caulobothrium Baer, 1948 or Rhabdotobothrium

Euzet, 1953, although adult cestodes classified in

these genera does not present the “apical sucker”,

perhaps due to the degeneration of this structure

during the development to the adult stage. Based on

the morphology and morphometrics of the

specimens here studied, their similarity with the

species of Echeneibothrium is considered. Healy et

al. (2009) refer that this genus of Echeneibothriinae

should be included in the new order

Rhinebothriidea Healy, Caira, Jensen, Webster &

Littlewood, 2009 (synonym of Tetraphyllidea

Carus, 1863 in part), with other five genera of

Echeneibothriinae, considering the bothridia with

stalks as observed in species of Echeneibothrium.

Comparison of larval Scolex spp. deposited in the

CHIOC, and recovered from fishes captured in the

littoral of Rio de Janeiro, with the specimens

studied here, similarities were observed in relation

to the plerocercoids of Scolex sp. (Scolex sp.2),

from Mugil platanus, by the presence of four

pedunculate bothrids with stalks, divided into 12

transversal extroverted loculi with apical

myzorhynchus as well as to the plerocercoids S.

pleuronectis recovered from Priacanthus arenatus

Cuvier, 1829; Katsuwonus pelamis (L.); Tylosurus

acus (Lacepède, 1803); Pseudopercis numida

Miranda-Ribeiro, 1903 and P. semifasciata

Felizardo et al.Cestodes of the flounder

120

Figure 7. Plerocercoid of Scolex pleuronectis.

Scale bar = 200 µm.

(Cuvier, 1829), that present bothria with retracted

stalks inside the scolex.

Other plerocercoids deposited in the CHIOC as

Scolex sp. and S. pleuronectis were also observed;

considering that the samples were devoid of

evaginated penduculate stalked bothria in the

scolex, they are to be reconsidered in other genera

apart from Rhinobothriidea sensu Healy et al.

(2009). Those metacestodes are deposited and

identified as Scolex sp. from Mugil platanus

Günther, 1880 (Scolex sp.1), from Orthopristis

ruber (Cuvier, 1830), Haemulon steindachneri

(Jordan & Gilbert, 1882), Oligoplites saliens

(Bloch, 1793) and as S. pleuronectis from

Pomatomus saltatrix (Linnaeus, 1766), M.

furnieri, Trichiurus lepturus Linnaeus, 1758,

Caranx latus Agassiz, 1831, Pagrus pagrus

(Linnaeus, 1758.), G. brasiliensis, Paralonchurus

brasiliensis (Steindachner, 1875), Scomber

japonicus Houttuyn, 1782, Balistes capriscus

Gmelin, 1789, Euthynnus alleteratus (Rafinesque,

1810), Sarda sarda (Bloch, 1793), S. brasiliensis,

Katsuwonus pelamis (Linnaeus, 1758), and

Anchoa tricolor (Spix & Agassiz, 1829) (CHIOC

36258, some hooks were observed in the specimen

of this sample).

High prevalence indexes of parasitism by this

cestode have been already reported by Silva et al.

(2000b) in T. lepturus (P = 96.3 %), Alves et al.

(2002a) in G. brasiliensis (P = 87.3 %), Alves et al.

(2003) in S. japonicus (P = 30 %), Alves et al.

(2004) in Urophycis brasiliensis (Kaup, 1858) (P =

36 %) and Luque et al. (2008) in Pseudopercis

numida (P = 43.6 %) and P. semifasciata (P = 53 %),

from the littoral of Rio de Janeiro, thus confirming

the present findings. Lower prevalence indexes

were reported by Knoff et al. (1997) (P = 4.7 %,

Scolex sp.1, and 0.7 %, Scolex sp.2) in Mugil

platanus, Luque et al. (2000) (P = 3.6 %) in C. latus,

Paraguassú et al. (2002) in P. pagrus (P = 5.5 %)

and Alves et al. (2005) in B. capriscus (P = 10.7%).

Previous data related to plerocercoids

morphologically similar to those of the present

study, namely Scolex sp.2 in Mugil platanus, and S.

pleuronectis in P. numida and P. semifasciata were

reported by Knoff et al. (1997) and Luque et al.

(2008).

Paralichthys isosceles is a new host record for

Scolex pleuronectis.

Considering that data on cestodes infecting

specimens of P. isosceles are unavailable, results of

the present investigation were compared to those

related to other species of Paralichthys from other

localities. Oliva et al. (1996) reported to adults of

Pseudophyllidea (= Diphyllobotriidea?) of an

unidentified genus, parasitizing the intestine of P.

adpersus (Steindachner, 1867), in the North of

Chile (P = 4.5 %, MA= 0.07) what differs from the

results here obtained, when plerocercoids of

Diphyllobothrium sp.1 and Diphyllobothrium sp.2

were recovered. Chilean authors have also referred

to metacestodes of Trypanorhyncha, a plerocercoid

of Nybelinia surmenicola Okada, 1929 and one

plerocercum of Lacistorhynchus dollfusi

Beveridge & Sakanari, 1987, whereas during the

present investigation, other seven different species

were recovered. The tetraphyllid S. pleuronectis

was referred in the intestine (P = 5.7 % and MA=

0.29), in the same infection site here considered,

but with remarkably higher parasitological

indexes.

Castilho-Sánchez et al. (1998) reported to

tetraphylid cestodes parasitizing specimens of

Paralichthys californicus (Ayres, 1859), from

Bahía de Todos Santos, Estero de Punta Banda,

Bahía de San Quintín, Baja California and Pacific

ocean in Mexico. Cestodes were found infecting

the stomach, intestine and ceca, with prevalence

ranging from 1 to 6, depending on the collection

area; higher parasitic indexes were similar to those

presently observed although with plerocercoids

morphologically different (four sessile bothridia).

Considering ichthyo-sanitary approaches, the

presence of Trypanorhyncha metacestodes in the

musculature is harmless to humans only affecting

the hosts besides the repugnant aspect conferred to

the meat, often rejected by consumers and thus

impeding its commercialization after the sanitary

inspection (São Clemente et al., 2004). Recent

studies dealing with medium sized or huge

Trypanorhyncha plerocerci as Molicola horridus

( G o o d s i r, 1 8 4 1 ) D o l l f u s , 1 9 4 2 a n d

Gymnorhynchus gigas Robinson, 1959, have

demonstrated that their ingestion can trigger

allergenic processes in humans (Gòmez-Morales et

al., 2008). The presence of medium sized

Trypanorhyncha plerocerci as those of P.

crassicolle, P. heteracanthum an C. gracilis, found

DISCUSSION

Neotrop. Helminthol., 4(2), 2010

121

parasitizing the flounders presently investigated,

even appearing with low parasitological indexes,

must be of concern, mainly considering the species

infecting the musculature (Dias et al., 2009, 2010).

Considering the occurrence of metacestodes in the

musculature of fish specimens, as those studied

now, it is suggested that the affected areas should be

removed in order to permit the commercialization

of the meat, in agreement with data after Amato et

al. (1990) and São Clemente et al. (2004).

The finding of Diphyllobothrium spp.

plerocercoids in the musculature of specimens of

the flounder, indicates the risk of human

contamination (Knoff et al. 2008), thus

emphasizing the importance of alerting the sanitary

inspection services and of adopting proper

procedures for the control of this zoonosis. In order

to avoid the spreading of helminth infections,

individual efforts have to be made aiming at the

change of acquired alimentary habits, mainly those

related to the ingestion of raw or poor cooked fish,

thus increasing the possibility of human infections

(McCarthy & Moore, 2000; Knoff et al., 2008).

To Flávia Garcia de Carvalho (Serviço de

Comunicação ICICT/Fiocruz), Heloisa Nogueira

Diniz (Serviço de Produção e Tratamento de

Imagens IOC/Fiocruz) for processing the figures,

Elizabeth Luz Sanchez Romani by translating the

abstract into Spanish, and to Conselho Nacional de

Desenvolvimento Científico e Tecnológico -

CNPq, Brazil, for partial financial support to R. M.

Pinto.

Felizardo et al.Cestodes of the flounder

122

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*Correspondence to author/ Autor para

correspondencia:

Marcelo Knoff

Laboratório de Helmintos Parasitos de

Vertebrados, Instituto Oswaldo Cruz, Avenida

Brasil 4365, Manguinhos, Rio de Janeiro, 21040-

900, Rio de Janeiro, Brasil.

Tel: +552125621462

Fax: +552125621511

E-mail/correo electrónico:

knoffm@ioc.fiocruz.br

Received August 31, 2010.

Accepted October 27, 2010.

126